Visual Grouping and the Focusing of Attention Induce Gamma-band Oscillations at Different Frequencies in Human Magnetoencephalogram Signals

Abstract

Neural oscillatory synchrony could implement grouping processes, act as an attentional filter, or foster the storage of information in short-term memory. Do these findings indicate that oscillatory synchrony is an unspecific epiphenomenon occurring in any demanding task, or that oscillatory synchrony is a fundamental mechanism involved whenever neural cooperation is requested? If the latter hypothesis is true, then oscillatory synchrony should be specific, with distinct visual processes eliciting different types of oscillations. We recorded magnetoencephalogram (MEG) signals while manipulating the grouping properties of a visual display on the one hand, and the focusing of attention to memorize part of this display on the other hand. Grouping-related gamma oscillations were present in all conditions but modulated by the grouping properties of the stimulus (one or two groups) in the high gamma-band (70-120 Hz) at central occipital locations. Attention-related gamma oscillations appeared as an additional component whenever attentional focusing was requested in the low gamma-band (44-66 Hz) at parietal locations. Our results thus reveal the existence of a functional specialization in the gamma range, with grouping-related oscillations showing up at higher frequencies than attention-related oscillations. The pattern of oscillatory synchrony is thus specific of the visual process it is associated with. Our results further suggest that both grouping processes and focused attention rely on a common implementation process, namely, gamma-band oscillatory synchrony, a finding that could account for the fact that coherent percepts are more likely to catch attention than incoherent ones.

Neural Dissociation between Visual Awareness and Spatial Attention

“…Therefore, the faint stimuli used here induced a weak yet reliable gamma-band response over the visual cortex. Similar parieto-occipital increases of gamma-band activity have been observed previously in the scalp MEG using visual stimuli at maximal contrast (Hoogenboom et al, 2006;Vidal et al, 2006;Siegel et al, 2007).…”

“…Our results thus confirm the involvement of gamma-band activity in both visual awareness and spatial attention. However, the results further show that distinct frequency components of the gamma-band response may support flexibly and simultaneously distinct cognitive functions (Vidal et al, 2006;Buschman and Miller, 2007). Such a frequency specialization suggests that gamma-band synchronization is not a monolithic mechanism in charge of a single cognitive function (Tallon-Baudry, 2004;Tallon-Baudry et al, 2005;Buzsaki, 2006).…”

“…A major difference between the present and other studies is that we used faint stimuli at threshold contrast (ϳ3%) and not at maximal contrast (Ͼ80%). The appearance of the faint stimuli triggered a detectable gamma-band response over the visual cortex but a weak one compared with the responses induced by stimuli at maximal contrast (Hoogenboom et al, 2006;Vidal et al, 2006;Siegel et al, 2007). Top-down attentional biases might take more time to modulate such a weak response.…”

Anticipation of natural stimuli modulates EEG dynamics: physiology and simulation

“…Previous reports on stimulus-locked spectral responses often used rather simple stimulus configurations like geometrical shapes (Busch et al 2004;Fründ et al 2007b) or gratings (Bodis-Wollner et al 2001;Busch et al 2006b;Fründ et al 2007a;Schadow et al 2007) and observed response frequencies between 30 and \90 Hz. Other studies that applied more complex stimuli (Busch et al 2006a;Gruber and Müller 2005;Lachaux et al 2005;Tallon-Baudry et al 1997;Vidal et al 2006) either did not observe stimulus-locked c responses at all, or did not find these responses to be modulated by experimental manipulations. Our results are in line with these findings in that we did not find any stimulus-locked c responses at all.…”

Traditional and New Principles of Perceptual Grouping

“…Grouping may be mediated by synchronization of activity between neurons representing different elements of a group. Although some neurophysiological recordings in animals (e.g., Castelo-Branco, Goebel, Neuenschwander, & Singer, 2000;Singer & Gray, 1995) and EEG recordings in humans (e.g., Tallon- -Baudry, 2006) have supported this idea, it remains a controversial hypothesis (e.g., Lamme & Spekreijse, 1998;Roelfsema, Lamme, & Spekreijse, 2004). Much of that evidence applies to limited types of grouping such as collinearity/continuity (e.g., Singer & Gray, 1995) or formation of illusory contours based on these features (e.g., Tallon-Baudry & Bertrand, 1999).…”